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Alfei, S.;  Schito, G.C. Synthesis of CNTs and Biogenesis of BNTs. Encyclopedia. Available online: (accessed on 23 June 2024).
Alfei S,  Schito GC. Synthesis of CNTs and Biogenesis of BNTs. Encyclopedia. Available at: Accessed June 23, 2024.
Alfei, Silvana, Gian Carlo Schito. "Synthesis of CNTs and Biogenesis of BNTs" Encyclopedia, (accessed June 23, 2024).
Alfei, S., & Schito, G.C. (2022, September 05). Synthesis of CNTs and Biogenesis of BNTs. In Encyclopedia.
Alfei, Silvana and Gian Carlo Schito. "Synthesis of CNTs and Biogenesis of BNTs." Encyclopedia. Web. 05 September, 2022.
Synthesis of CNTs and Biogenesis of BNTs

Nanotubes (NTs) are mainly known as materials made from various substances, such as carbon, boron, or silicon, which share a nanosized tube-like structure. Among them, carbon-based NTs (CNTs) are the most researched group. CNTs, due to their nonpareil electrical, mechanical, and optical properties, can provide tremendous achievements in several fields of nanotechnology. Unfortunately, the high costs of production and the lack of unequivocally reliable toxicity data still prohibit their extensive application. A significant number of intriguing nanotubes-like structures were identified in bacteria (BNTs). The majority of experts define BNTs as membranous intercellular bridges that connect neighboring bacterial cell lying in proximity. Most evidence suggested that bacteria exploit NTs to realize both antagonistic and cooperative intercellular exchanges of cytoplasmic molecules and nutrients. Among other consequences, it has been proposed that such molecular trade, including even plasmids, can facilitate the emergence of new non-heritable phenotypes and characteristics in multicellular bacterial communities, including resistance to antibiotics, with effects of paramount importance on global health.

carbon nanotubes (CNTs) bacterial nanotubes (BNTs) Synthesis

1. Introduction

Nanotechnology is an area of research and manufacturing technology of global interest, which deals with a variety of materials produced at a nanometer scale (<100 nm) through different chemical and physical methods [1]. Nanotubes (NTs) belong to a promising group of nanomaterials which allows approaching several new electronic, magnetic, optical, and mechanical properties [2].
Even though many NTs containing boron, silicon, and molybdenum have been extensively studied, currently, carbon nanotubes (CNTs) are the most researched group among existing NTs structure [2]. Indeed, as it was evidenced by a search made on Scopus by using as keywords first “nanotubes” and then “carbon nanotubes”, in the last two decades (2001–2021) up to 182,033 documents concern nanotubes of which 145,162 (80%) concern carbon nanotubes.
CNTs are composed of graphite sheets rolled up in an unbreakable and non-stop hexagonal-like lattice structure, in which carbon atoms appear at the tops of the hexagon-type forms. Based on the number of carbon sheets, CNTs are categorized as single wall carbon nanotubes (SWCNTs), double wall carbon nanotubes (DWCNTs), and multi-wall carbon nanotubes (MWCNTs) [2]. CNTs belonging to all categories vary by purity, length, and functionality, but possess a plethora of properties, including high electrical conductivity, high tensile strength, light weight [2][3][4][5], high biocompatibility [6], capability of molecules immobilization for their transportation, large surface area, chemical inertness, possible presence of functional groups, elasticity, thermal conductivity and expansion, electron emission capacity, and high aspect ratio [2][3][4][5].
The unique composition, geometry, and properties of CNTs enable numerous potential applications. A great challenge of researchers in the field consists of reducing costs of CNTs production down to commercially viable levels, and it seems that scaling up in their synthesis is happening. CNTs can be applied for energy storage, biomedical uses, air, and water filtration. Additionally, CNTs can be used as molecular electronics, thermal materials, structural materials, electrical conductors, fabrics and fibers, catalyst supports, conductive plastics, conductive adhesives, as well as ceramics [2].
Interestingly, CNTs have great potential to be applied in nanomedicine for disease diagnosis and drug targeting, as well as to transport various biomolecules, such as proteins, DNA, RNA, immune-active compounds, and lectins [7][8].
CNTs are also extensively applied to develop electrochemical sensors, DNA-based sensors, as well as piezoelectric and gas sensors [2]. Additionally, opportunely structured CNTs, such as cationic CNTs have revealed to possess interesting antibacterial and antifungal activity [2].
A multitude of other possible applications for CNTs exist, as solar collectors, catalyst supports, nano-porous filters, and coatings of all types. Surely, many unexpected applications for these amazing materials will occur in the next years, which will confirm how CNTs could be the most important and valuable nanomaterial ever used. Several experts in the field are thinking to use CNTs for obtaining conductive and/or waterproof paper. CNTs possess the capability to absorb infrared light and may be applied in the I/R Optics Industry. To avoid tedious repetitions, more information and more exhaustive literature data concerning the potential applications of CNTs will be provided in the following parts. Intriguingly, nanostructures referred to as nanotubes exist also in the world of living beings. In eukaryotic cells, nanotubes promote intercellular transport of cytoplasmic substances, organelles, membrane constituents, as well as pathogenic microorganisms, including viruses [9]. Additionally, even if contrasting opinions and findings are emerged recently, it was reported that bacterial cell–cell interactions are mediated by tubular protuberances, labeled nanotubes, by similarity to their eukaryotic counterparts [10]. Indeed, it has been reported that bacteria, in addition to keep complex molecular exchanges and correspondence with neighboring eukaryotic and prokaryotic cells, by specific apparatuses including type III, IV, and VI secretion systems [11][12], they also mediate contact-dependent interactions by nano-membranous tubular conduits (namely nanotubes), which bridge neighbouring or distant cells of same or different species [10][13].

2. Synthesis of CNTs

2.1. Arc Discharge (AD)

In 1991 during an AD process intended to produce fullerenes using a current of 100 amps, the formation of CNTs in the carbon soot of graphite electrodes was detected [14]. Subsequently, by the same method the first macroscopic production of CNTs was made in 1992 [15]. The high temperatures (> 1700 °C) used in this method for CNTs synthesis typically causes the CNTs’ expansion, and CNTs are obtained with less structural defects in comparison with other methods [16].

2.2. Laser Ablation (LA)

This process, was developed by Dr. Richard Smalley and co-workers at Rice University, who produced different metal molecules by blasting metals with a laser. By replacing the metals with graphite, they succeeded in creating first MWCNTs [17], and later SWCNTs using a composite of graphite and a cobalt/nickel mixture as metal catalyst particles [18].

2.3. Chemical Vapor Deposition (CVD)

CVD is the most widely used method to produce CNTs [19] consisting of preparing first a substrate of metal catalyst NPs of nickel, cobalt, iron, or a combination [20][21] in the reactor by several possible ways, including reduction in oxides or oxides solid solutions and heating such a substrate at approximately 700 °C. Then, the growth of CNTs is triggered by bleeding into the reactor a “process gas”, such as ammonia, nitrogen, or hydrogen, and a “carbon-containing gas”, such as acetylene, ethylene, ethanol, or methane. CNTs develop at the locations of the metal catalyst particles, which can move at the top of the growing CNT during its growth or remain at the CNT base [22][23]. To increase the surface area for achieving higher yields of the catalytic reaction, the metal NPs can be mixed with a catalyst support, such as MgO or Al2O3. Thermal catalytic decomposition of hydrocarbon can be a promising route for the bulk production of CNTs. The most widely used reactor for preparing CNTs by CVD method is the fluidized bed reactor. The main drawback of CVD technique when support for catalyst NPs is used is the need of removing the catalyst support via an acid treatment, which sometimes could destroy the original structure of the CNTs [19][24]. Interestingly, an advanced CVD technique, namely plasma-enhanced chemical vapor deposition (PECVD) consists of generating a plasma by the application of a strong electric field during growth. In this case, the CNT growth will follow the direction of the electric field [25]. By adapting the reactor’s geometry, it is possible to synthesize vertically aligned CNTs [26], whose morphology is of interest to researchers interested in electron emission from nanotubes. Among the various methods to synthetize CNTs, CVD is the most suitable for scaling-up and industrial production, due to its low cost, and the possibility of growing nanotubes directly on a desired substrate by careful deposition of the catalyst [27].

High-Pressure Carbon Monoxide (HiPco) Process

In the HiPco process developed at Rice University, SWCNTs are created from the gas-phase reaction of iron pentacarbonyl with high-pressure carbon monoxide (CO) gas. Particularly, iron NPs are produced that provide the nucleation surface for the transformation of CO into carbon during the growth of the CNTs. Experiments were made using material in quantities of milligrams to grams. Waste material was regularly removed by a professional company, and incinerated, avoiding environmental release [28].

Super-Growth CVD

Super-growth CVD (SGCVD), also known as water-assisted chemical vapor deposition, developed by Kenji Hata, Sumio Iijima, and co-workers at AIST (Japan) [29], uses water into the CVD reactor, to improve the activity and lifetime of the catalyst. This process allows to obtain either dense millimeter-tall vertically aligned nanotube arrays (VANTAs) or “forests”, which are aligned normally to the substrate. The synthesis efficiency is about 100 times higher than that of the LA method, and SWNT forests of 2.5 mm height can be made in 10 min. SWNT forests can be easily separated from the catalyst, yielding clean SWNT material (purity > 99.98%) without further purification, differently from the CNTs obtainable by the above-reported HiPco process, which could contain 5–35% of metal impurities; and need purification work-up through dispersion and centrifugation that damages the nanotubes [28]. The mass density of SGCVD-based CNTs is much lower than that of conventional CNT powders, probably because the latter contain metals and amorphous carbon. The vertically aligned nanotubes forests originate from a “zipping effect” caused by the surface tension of the solvent and the Van der Waals forces between the CNTs when they are immersed in a solvent and dried. VANTAs can be formed in various shapes, such as sheets and bars, by applying weak compression during the process. The packed CNTs are more than 1 mm long [30].

2.4. Other Methods

Plasma Torch (PT)

Plasma torch for producing SWCNTs was developed by Olivier Smiljanic in 2000 at Institut National de la Recherche Scientifique (INRS) in Varennes, Canada. A mixture of argon, ethylene and ferrocene is introduced into a microwave PT, where it is atomized by the plasma at atmospheric pressure, which has the form of an intense ‘flame’. The fumes created by the flame contain SWNTs, metallic and carbon nanoparticles, and amorphous carbon [31][32]. The decomposing of the gas can be 10 times less energy-consuming than graphite vaporization, as made in LA or AD. SWCNTs were obtained by a modified PT method namely ITP method, implemented in 2005 by groups from the University of Sherbrooke and the National Research Council of Canada [33]. As in AD, an ionized gas is used to reach the high temperature necessary to vaporize carbon-containing substances and the metal catalysts necessary for the ensuing nanotube growth. The thermal plasma is induced by high-frequency oscillating currents in a coil and is maintained in flowing inert gas. SWCNTs with different diameter distributions can be synthesized.

Liquid Electrolysis Method (LEM)

MWCNTs can be obtained by electrolysis of molten carbonates [34], with a mechanism like that of CVD. In this case, metal ions were reduced to a metal form and attached on the cathode forming the nucleation point for the growing of CNTs. The net reaction is:
Fibers 10 00075 i001
Practically, the reactant is only greenhouse gas of carbon dioxide, while the product is high valued CNTs. This discovery represents a possible technology for carbon dioxide capture and conversions [35][36][37][38].

Natural, Incidental, and Controlled Flame Environments

Note that CNTs are commonly formed in commonplace flames produced by burning methane, [39] ethylene, [40], and benzene [41], and they have been found in soot from both indoor and outdoor air [42]. Unfortunately, these naturally occurring CNTs are highly irregular in size and quality because produced is uncontrolled conditions, and lack in the high degree of uniformity necessary to satisfy the many needs of both research and industry. Recent efforts have focused on producing more uniform carbon nanotubes in controlled flame environments [43][44][45][46][47]. Such methods have promise for large-scale, low-cost nanotube synthesis based on theoretical models though they must compete with rapidly developing large scale CVD production.

3. Biogenesis of Bacterial Nanotubes: Among Sheared and Conflicting Opinions

By using B. subtilis, Dubey et al. reported that BNTs exist both as intercellular tubes connecting neighboring bacterial cells and as elongated extending tubes, connecting distant bacterial cells [12]. In this regard, it is reported that the latter are produced by bacteria when grown at low density [12]. Additionally, the Dubey group identified a phosphodiesterase calcineurin-like protein, namely YmdB, present both in the cytoplasm and in nanotubes. YmdB is highly conserved among Gram-positive and Gram-negative bacteria and it was demonstrated that it is an essential factor for nanotubes formation and intercellular molecular exchange. Enzymatic analysis and crystal structure of YmdB evidenced that it has a metallophosphodiesterase conserved domain, that serves to hydrolyze cyclic AMP (cAMP) [48][49], which work as secondary messengers to control the social activities and the proper colony development in microbes [50][51][52][53]. Diethmaier et al. in 2014 described an additional effect of YmdB on mRNA levels of many genes, including those involved in motility, biofilm formation, and sugar utilization [49]. YmdB induces the expression of biofilm matrix genes and repress the expression of motility genes, hence controlling the switch from a motile to a multicellular sessile lifestyle [48]. Further investigations suggested that the effect of YmdB on nanotubes is independent of its role in biofilm development. Alternatively, the formation of nanotube networks might be a preceding stage in the establishment of a biofilm, providing the foundation for unhampered intercellular molecular flow between its inhabitants. Concerning the subcellular localization of YmdB, it was demonstrated that it preferentially locates to the cell circumference, often concentrated in foci-like assemblies in a frequency of approximately one per cell. Therefore, YmdB is mainly in the cytoplasmic fraction associated with the membrane. An abundance of YmdB was detected also in the nanotube fraction. Indeed, it was observed that YmdB molecules clearly coincided with nanotubes and specifically co-localize with nanotubes [13]. Collectively, it was uncovered that YmdB is associated both with the cell periphery and nanotubes. Practically, YmdB positioned to the periphery of bacterial cell hydrolyzes cAMP deriving from external sources, thus transmitting a message to produce BNTs. Furthermore, YmdB situated in the emerging nanotubes serve to feel neighbor cells and direct the tube growth toward the detected stimulus. Additionally, this external signal also regulate YmdB subcellular localization, creating high local concentrations of protein molecules, that subsequently recruit additional nanotube machinery components.
Estimates of the number of bacteria cells producing NTs evidenced that 95% of the wild-type (WT) cells showed nanotubes, whereas less than 5% of mutant cells not possessing YmdB held NTs [54].
In addition to YmdB, flagellar body proteins called CORE, which are required for the flagellar export apparatus [13][55] have been reported to be necessary for BNTs formation in B. subtilis, and, therefore, they operate both in flagella and in BNTs assembly [13][55][56].
Particularly, Bhattacharya et al., using B. subtilis revealed that conserved components of CORE, dually serve for flagellum and nanotube assembly [55]. Particularly, flagellar CORE apparatus consists of a group of transmembrane proteins, particularly FliP, FliQ, FliR, FlhB, and FlhA in ratio 5:4:1:1:9, and of the chaperone FliO, since only transiently it associates with the CORE complex.
In this regard, the researchers demonstrated that mutant bacteria, also of different species lacking CORE genes, even if gifted with other flagellar components, do not produce nanotubes and are not able to carry out intercellular molecular trafficking, thus establishing that formation of BNTs mediated by CORE is ubiquitous and is universal and phylogenetically widespread.
Additionally, they evidenced that the CORE components are located where the nanotube emerges analogously to what was already observed for the flagella, and that exogenous COREs deriving by different species could restore nanotube generation and functionality in bacteria lacking endogenous CORE [55].
Recently, other genes required for NT formation were detailed using a systematic, unbiased approach [54], which allowed to identify the regulon that contains genes necessary for NTs formation. In this regard, although with no statistical significance, due to the low number of NTs produced in the tested conditions, it was determined that among the 19 sigma factors of WT B. subtilis the sigma factor, namely SigD, is required for NTs formation and was identified as the above-mentioned regulon, from which CORE genes depend [54]. As confirmation, exponential phase ΔsigD cells (not possessing SigD), differently from WT cells did not produced NTs within a 15 min time course experiment [54]. It was evidenced that other gene from the SigD regulon besides the CORE ones are involved in NTs formation [54]. It was demonstrated that autolysins-peptidoglycan hydrolases, such as LytE, LytF, LytB, and LytC, that open connections in the peptidoglycan net, thus allowing the insertion of afresh synthesized material for permitting surface expansion and cell separation [57], could be involved in the formation of BNTs, by weakening peptidoglycan and allowing BNTs extrusion [58]. In this regard, it was reported that in ΔsigD or ΔlytEF mutant cells the blockage of the cell wall degradation by the lack of LytE and LytF caused the delay in the appearance of NTs, while ΔlytBC mutant displays reduced NT production [58].

Recent Reports on Conditions and Requirements Promoting NT Formation

Using a combination of structured illumination microscopy (SIM) and scanning electron microscopy (SEM), it was possible to observe that, in B. subtilis cells (BSB1) grown to exponential phase, two types of filamentous structures were present. Particularly, several thinner filaments (diameter < 30 nm) and few thicker ones (diameter ~70 nm), identified as NTs, were observed [54]. Among the filaments believed to be NTs, elongated, flattish terminal structures were observed, but, collectively, the frequency of NTs was rather low. Only one NT approximately per 500 cells was observed, and, while a cell can have many flagella, only one nanotube, when present, is typically possessed by B. subtilis. Additionally, it was demonstrated that the amounts of NTs observed are sensitive both to growth conditions (solid or liquid media) and to the conditions used for preparation of the microscopic samples. Particularly, cells grown in liquid media displayed few NTs, while cells grown on solid media formed either no NTs or many NT-like structures depending on the sample preparation protocols [54]. Additionally, it was observed that the cells possessing NT structures were not in health cells. Particularly, it has been demonstrated that under non-stress conditions, NTs are uncommon; while under stress, the number of NTs increases. Indeed, it was observed that while in non-stress conditions no NT was detectable in WT B. subtilis cells from the exponential phase, in stress conditions by using glass slides and coverslips coated with poly-L-lysine (which negatively impacts with bacteria grow) a few NTs were observed, whose number increased when the coverslip was firmly pressed down [54]. Intriguingly, differently from Dubey et al., which indicated that NTs were formed by intact living cells [13], recently it was demonstrated that NTs structures are formed when cells are dying or even after cell death, regardless the stress applied to cause cell death, including pressure or different antibiotics. This finding established that NTs are improbable to be involved in the uptake of nutrients or in the exchange of cytoplasmic content as proposed by previous studies [54]. Experiments demonstrated that severe damage to bacterial cells resulted both in larger amounts of dying cells and NTs production, because of the compromised cell wall and (likely) excess internal pressure. Importantly, according to recent findings, NTs do not serve as channels through which nonconjugative plasmids can be transported, but they are a sign of disintegrating cells, and further studies are necessary to assess a probable physiological role of NTs. Time-lapse microscopy experiments have demonstrated that NTs formation is a rapid process, in the order of seconds, during which the NTs use the cell plasma membrane for their extrusion. It was proposed, that since the cells are dying and start collapsing, weak spots in the cell wall may operate as channels through which NTs are extruded to release the intracellular pressure, and cardiolipin which is an integral part of the B. subtilis membrane might play a role in NT formation [59][60]. Indeed, it was observed that cardiolipin combined with the PmtA protein from the phytopathogenic bacterium Agrobacterium tumefaciens was previously reported to promote formation of tubular structures in vitro [61].

Not Only in B. subtilis

In addition to B. subtilis, membranous tubular structures inducted by some type of stress and emerging from dying cells have been detected also in other bacterial species, such as B. megaterium, D. radiodurans, and E. coli, and in eukaryotic cells, such as macrophages. Particularly, B. megaterium is rapidly inhibited by B. subtilis by delivering the tRNase toxin WapA and by nutrients extraction utilizing the same nanotube apparatus in a bidirectional manner, to maximally exploit potential niche resources [62].
Interactions within and between Acinetobacter baylyi and E. coli, in which two distant bacterial species can connect each other via membrane-derived nanotubes and use these to exchange cytoplasmic constituents, such as amino acids, have been reported when auxotrophy-causing mutations were induced [63]. Tubular structures, termed outer membrane tubes (OMTs), induced by stress, such as lack of oxygen or addition of metabolic inhibitors, have been observed in M. xanthus [64][65]. OTMs contain outer membrane (OM) proteins and lipids and no other cytoplasmic material and are not involved in the intercellular transfer of OM proteins, which instead depends on the TraAB system and direct cell-to-cell contact. On the contrary, Wei et al. [66] reported that OMTs are predominantly associated with ghost cells. Additionally, OMTs were also found in F. novidica and F. tularensis when subjected to conditions of stress induced by amino-acids deprivation or during infection by macrophages [66][67]. Nevertheless, these structures, being formed from the OM, do not have to cross the cell wall and, consequently, the mechanism of their formation is different from that of production of BNTs in B. subtilis. Finally, NTs-like structures were observed in D. radiodurans when stressed with mitomycin C [68]. Various types of tubular structures have also been reported for eukaryotic cells and mitochondria, in some cases, paradoxically induced by the presence of bacteria. Tunneling nanotubes (TNTs) of macrophages are an example [69][70]. TNTs are long-range membranous F-actin containing tube-like structures, that have been classified into two types based on their thickness and the presence or absence of microtubules [71], whose formation can be inducted by HIV-1 virus whose formation is stimulated by coinfection with M. tuberculosis [72]. TNTs, however, appear to be distinct from bacterial NTs by the presence of a protein scaffold and appear to be channels for cell-to-cell communication. Collectively, it can be assumed that B. subtilis NTs are a trait of dying cells, or cell death, and are involved in the final cell collapse. In other bacterial species, similar structures should be studied with utmost care before attributing physiological roles to them.


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